title: effects of temperature and salinity on the survival and
TRANSCRIPT
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Title: Effects of temperature and salinity on the survival and 2
development of larval and juvenile Palaemon serratus 3
(Decapoda: Palaemonidae) from Irish waters 4
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Authors: Eoghan Kelly1, Oliver Tully1 and Ronan Browne2 6
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Key words: Palaemon serratus; Larvae; Juveniles; Temperature; Salinity; Development, Survival 8
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Postal Addresses of Affiliations: 10
2 National University of Ireland, Galway 11
1Marine Institute, Rinville, Oranmore, Galway, Ireland 12
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E-mail: [email protected], [email protected], [email protected] 14
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ABSTRACT 18
The combined effects of temperature and salinity on the survival and development of larval and 19
juvenile Palaemon serratus from the west coast of Ireland were investigated. Survival over time was 20
measured at thirty combinations of temperature and salinity ranging from 10-19°C and 9-34‰ in a 21
fully factorial design. Salinity had a stronger influence than temperature on survival at all larval 22
stages except stage V. For juveniles the main effect changed from temperature between 100–200 23
degree days to salinity between 200–600 degree days and temperature between 600 and 800 degree 24
days. Estimates of time taken to 50% mortality showed that juveniles tolerated lower salinities for 25
longer periods and exhibited optimal salinity values which were 3‰ lower than larvae, at 26
temperatures between 10–15°C. Larval stage durations were found to be influenced by temperature 27
but not salinity. Comparison with published data suggests that populations of P. serratus have 28
adapted to local conditions of temperature and salinity. The results presented here have practical 29
implications for fisheries assessment and management, as the incorporation of environmental 30
effects into stock-recruitment models can improve their predictive capacity. 31
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INTRODUCTION 34
Decapod shrimps and prawns are an important component of coastal ecosystems as they provide a 35
crucial link between the micro and macro trophic levels by feeding on algae, bryozoans, small 36
crustaceans, molluscs and polycheates and in turn are predated on by various species of fish and 37
birds (Smaldon, 1993). Palaemon serratus (Pennant, 1777) is a coastal species of shrimp found in 38
the Mediterranean, Black Sea and Atlantic Ocean from Mauritania to Denmark and is at the 39
northern limit of its range around Ireland. It is harvested across this range and the commercial 40
fishery in Irish coastal waters removed between 150–550mt per year between 1990-2006. This 41
catch represented an annual removal of 29–66% of the spawning stock biomass between 2005-2006 42
depending on region (Kelly et al., 2009). Irish landings of this species increased throughout the 43
1990s, although since 1999 the general trend has been downwards, with large inter-annual 44
fluctuations in catch rates and landings (Fahy & Gleeson, 1996; Kelly et al., 2009). The reasons for 45
these fluctuations are not known, but may be due to inter-annual variability in recruitment either 46
because of restricted spawning output, as a result of excessive fishing or natural mortality on mature 47
adults, or due to variability around the stock-recruitment relationship caused by environmental 48
effects acting on early life history stages. 49
50
The life cycle of P. serratus includes a planktonic larval phase and demersal juvenile and adult 51
phases (Smaldon, 1993). Larvae hatch from May onwards and are common in inshore surface 52
waters in July (Figueras, 1987). The number of larval stages is variable depending on 53
environmental conditions but typically there are eight or nine (Fincham & Figueras, 1986). Late 54
stage larvae settle into shallow sub tidal habitats in late July and August (Forster, 1951; 55
DeBhaldraithe, 1971) and appear in the fishery in mid October (Kelly et al., 2009). Over this 56
developmental period the larvae and juveniles are exposed to large variations in temperature and 57
salinity due to the effects of solar heating, evaporation, rainfall and river flow (Figueras, 1987). 58
These environmental variables have previously been shown to have significant effects on the 59
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survival, metabolism and growth of P. serratus larvae in the Mediterranean (Yagi & Ceccaldi, 60
1984; Yagi & Ceccaldi, 1985; Yagi et al., 1990). 61
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Palaemonid shrimp have body fluids that are hypotonic to seawater and must hyporegulate in order 63
to maintain the correct ionic balance (Panikkar, 1941; Parry, 1954; Spaargaren, 1972). When 64
exposed to salinity outside of their optimum range they spend an increasing amount of energy on 65
osmoregulation to maintain homeostasis. This energy demand is at the expense of other metabolic 66
functions and if the environmental conditions deviate too far from the optimum, homeostasis cannot 67
be maintained and the animal dies. In general the Palaemonid family of shrimp exhibit well 68
developed hyper- and hypo-osmotic regulatory capabilities in mid-range salinities (Freire et al., 69
2003). However, P. serratus is a marine species (Smaldon, 1993), which only enters estuaries 70
temporarily prior to larval release. Consequently, it has a higher iso-osmotic point and a more 71
restricted osmoregulatory range than the fully estuarine Palaemon longirostris and Palaemon 72
macrodactylus (Gonzalez-Ortegon et al., 2006). The influence of salinity on the rate of respiration 73
in the larvae of P. serratus from the Mediterranean was found by Yagi et al. (1990) to have a 74
quadratic shape with lower metabolic rates, as measured by oxygen consumption, occurring at both 75
low (13‰) and high (43‰) salinities with the optimum between 25–31‰. 76
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As with all ectotherms, the body temperature of P. serratus, and hence its metabolic rate, is 78
dependent on ambient temperature. The relationship between metabolism and temperature is 79
positive, but non-linear, with an upper and lower limit. In larval P. serratus the maximum 80
metabolic rate of physiological processes, such as osmoregulation, was found by Yagi et al. (1990) 81
to occur at 29ºC. Combinations of low temperature and low salinity have a doubly negative effect 82
on the growth and survival of P. serratus larvae (Yagi & Ceccaldi, 1985). 83
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Off the south coast of Ireland, the average sub-surface water temperatures during the larval and 85
post-larval period from May to July ranged from 12–15ºC (Marine Institute data 2004-2006). In 86
contrast the optimal temperature for rearing P. serratus in the UK was estimated by Reeve (1969b) 87
to be in the range 22–26ºC, and larval survival was reduced and development was prolonged at 88
lower temperatures. Sub-surface salinity off the south coast of Ireland during April and May 89
(Marine Institute data 2003–2007) was 26–35‰. In addition the annual rainfall data on the south 90
coast (Met Eireann data 1998–2004) displayed 42% variation in annual precipitation which suggests 91
that there is significant interannual variation in salinity in coastal and estuarine areas. It is therefore 92
likely, given the published data, that temperature and salinity conditions in Irish waters are sub-93
optimal for development and survival of P. serratus unless these populations have specifically 94
adapted to these conditions. 95
96
The purpose of the present work was to model the survival of larvae and juveniles of P. serratus 97
hatched from mature berried females taken in Irish waters over a range of temperature and salinity 98
conditions which reflect those in Irish coastal waters. Previous work on the related species P. 99
adspersus and P. squilla (Berglund & Lagercrantz, 1983) showed adaptation of shrimp populations 100
to local environmental conditions and significant genetic differences existed between populations 101
along the European Atlantic coast. A comparison of the effects of temperature and salinity on 102
larval development and survival in populations of P. serratus from Ireland and the Mediterranean 103
might indicate if they have adapted to local conditions. Adaptive genotypic or phenotypic plasticity 104
is an important feature of species physiology in coping with environmental change, at any given 105
location, and in determining its overall geographic range (Gotthard & Nylin, 1995). 106
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MATERIALS AND METHODS 108
Re-circulating Aquaculture System (RAS) 109
Adult shrimp were sourced from Rossaveel, Co. Galway on the mid west coast of Ireland and were 110
transferred directly to a laboratory at Carna, Co. Galway. Here the ovigerous females were 111
removed and divided equally between 5 independent, 250L, thermostatically controlled, re-112
circulating aquaculture systems (RAS). The water temperatures were set at 10˚C, 12˚C, 15˚C, 17˚C 113
and 19˚C and the brood-stock was fed to satiation with pelleted food (Frippak Ltd. ‘Breed Shrimp’). 114
A light:dark cycle of 10:14 hours was maintained. Cannibalism and physical injury in the holding 115
tanks due to aggressive behaviour (Reeve, 1969a) was minimised by the use of AquaMatTM artificial 116
seaweed. During the brood-stock holding period the temperature, dissolved oxygen, salinity and 117
ammonia levels were recorded on alternate days. Temperature, salinity and DO were monitored 118
using a multi-probe (YSI 2500) while ammonia concentration was determined using a hand held 119
colorimeter (Hach DR/850). 120
121
Embryo development was monitored by viewing egg samples under a binocular microscope 122
(Philips, 1971). When well developed embryos were observed, a 70L larval collection device was 123
positioned underneath the outflow pipe from the main tank to collect larvae that were passively 124
removed from the brood tank. To ensure that the larvae at the start of an experiment were at the 125
same age, only larvae that hatched on the day prior to the beginning of the experiment were used. 126
127
Water quality parameters 128
Average water temperature over the brood stock holding period (17 February to 3rd May 2005) for 129
each RAS was 9.1˚C, 11.6˚C, 15.2˚C, 16.7˚C and 18.8˚C. Dissolved oxygen (DO) values were 130
higher at lower temperatures with an average of 7.6mg.L-1 at 10˚C and 6.1mg.L-1 at 19˚C. Levels of 131
DO for the 12˚C, 15˚C and 17˚C were in between these two extremes. In general it is recommended 132
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that DO levels in RAS be maintained at >5mg.L-1 (Timmons et al., 2002). Recorded values for 133
salinity in the brood-stock holding systems showed a significant (p<0.01) relationship with 134
temperature which was possibly due to evaporation. Mean salinity at 10˚C and 19˚C was 34.8‰ 135
and 36.6‰ respectively, with standard deviations across all RAS ranging from 0.42–0.86‰. The 136
ammonia concentration showed no clear relationship with temperature and mean values ranged 137
from 0.21±0.17mg.L-1 to 0.29±0.26mg.L-1. A maximum of 1.05mg.L-1 was recorded at 17˚C. This 138
value is a factor of 10 lower than the lethal limit for adult P. serratus of 10mg.L-1 (Reeve, 1969a). 139
Water temperatures recorded over the experimental period, 11th April to 26th August 2005, fell 140
within 0.2˚C of the target with standard deviations of between 0.3˚C and 0.6˚C. 141
142
Larval experimental design 143
The temperature control systems for the larval experiments were set at 10˚C, 12˚C, 15˚C, 17˚C and 144
19˚C. Each system contained 6 experimental vessels containing 1.5L of diluted seawater at a 145
salinity of 9‰, 14‰, 19‰, 24‰, 29‰ and 34‰. This resulted in a total of 30 temperature/salinity 146
combinations in a fully factorial, non-replicated experimental design. This range of temperature 147
and salinity was selected as it encompassed the environmental conditions likely to be experienced 148
by larvae and juveniles in Irish waters during May and June. One hundred larvae at zoeal stage I 149
were transferred into each of the 30 experimental vessels. To avoid temperature shock the larvae 150
were sourced from the rearing systems at the same temperature as the experiments. Aeration was 151
provided to each vessel and the rate of airflow was controlled to ensure a steady stream of bubbles. 152
The shrimp larvae were supplied with live nauplius stage brine-shrimp (Artemia salina) at a density 153
of ~10ml-1. To ensure maximum nutritional value, and to reduce the risk of bacterial (eg. Vibrio 154
spp.) infection, the Artemia cysts were decapsulated prior to incubation using sodium hypochlorite. 155
156
Numbers of viable larvae remaining in each experimental vessel were counted on alternate days. 157
After counting, a sub-sample was viewed under a binocular microscope to determine the average 158
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larval stage (Fincham & Figueras, 1986). After counting and staging, the larvae were returned to 159
the experimental vessel with water at the original temperature and salinity, and re-supplied with 160
Artemia at the correct density. 161
162
Juvenile rearing 163
When larvae were to be on-grown to juveniles, they were removed from the larval collection system 164
and transferred to a static 70L vessel containing sea water at salinity of ~34‰. These rearing tanks 165
were supplied with moderate aeration and immersion heaters which maintained the temperature at 166
~20˚C. Brine-shrimp nauplii (Artemia salina) were prepared and added in the same manner as 167
described for the larvae. In addition 3L of mixed algal culture (Tetraselmis sp., Isocrysis sp. and 168
Nannochloropsis sp.) was added to each rearing tank. These algal species have been shown to 169
protect against disease, to enrich the nutritional content of the Artemia and to stimulate larval 170
feeding (Duerr et al., 1998; Soares et al., 2006). 171
172
Previous work on the rearing of P. serratus larvae by Reeve (1969a) showed that the time taken 173
from hatching to juvenile metamorphosis is a function of temperature and takes approximately 600 174
degree days. Degree days is the product of the number of days and temperature, and it is a 175
necessary standardization because metabolism in exothermic animals, and hence the rate of 176
development, is a function of temperature. Larvae at zoeal stage I were added to each rearing tank 177
over a period of 6 days, after which a new tank was set up for subsequent batches of larvae. 178
Separation of ages minimised the risk of cannibalism. Water quality was maintained by draining 179
and refilling the rearing tanks on alternate days. Artemia nauplii and mixed algal culture were 180
resupplied as described above. 181
182
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Juvenile experimental design 183
Before starting the juvenile experiments, a sub-sample was placed on a 1mm Sedgewick-Rafter 184
Counting Cell (Pyser SGI Ltd.) and viewed under binocular microscope in order to determine the 185
average size. Sixteen percent of the juveniles used in the experiments (240/1500) were measured. 186
The average total length ± standard deviation was 9.0 ± 0.7mm with a range of 7–11mm. 187
Temperature and salinity conditions for the juvenile experiments were the same as those used in the 188
larval experiments. The experimental vessels were modified by the addition of a single strip of 189
AquaMatTM (~20cm long by 1cm wide). This provided the juveniles with a surface to settle on and 190
was weighted at one end so that it floated vertically in the experimental vessel. Artemia feeding 191
rates were the same as for larvae (~10 per ml), however, a small amount of prepared food (INVE 192
Aquaculture Ltd. Product: PL+500) was also added. Fifty juveniles were introduced at the start of 193
each experiment and the water was changed every other day at which time surviving juveniles were 194
counted. 195
196
As age increased in the experiments, the variation in the moult-stage distribution also increased due 197
to individual variation in the inter-moult period. In the larval experiments this developmental 198
process was accounted for by following the numbers at each zoeal stage. However, juveniles do not 199
exhibit discrete morphological changes as they grow. Consequently, selecting a point in time from 200
the continuous time series of juvenile data to draw samples was more subjective. Samples were 201
extracted at 100, 200, 400, 600 and 800 degree days. 202
203
Modeling the experimental results 204
The numbers of larvae and juveniles surviving over time were plotted as wire-frame, three-205
dimensional charts: x (temperature), y (percentage surviving), z (salinity ). A temperature/salinity 206
response surface model was then fitted to the x, y, z data so that larval and juvenile survival over 207
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time could be predicted over the range of temperature and salinity conditions covered in the 208
experiments. In addition, the regression and ANOVA outputs of this analysis revealed which 209
variable, or combination of variables, had the greatest effect on mortality. A quadratic model of the 210
following form was fitted to the data: 211
y = a + (B1x1) + (B2x2) + (B11x12) + (B22x2
2) + (B12x1x2) (1) 212
Where: y = larval/juvenile numbers, B1 = Factor 1 (i.e. Temperature), B2 = Factor 2 (i.e. Salinity), 213
B11 and B22 = Quadratic terms (i.e. ‘Temperature2’ or ‘Salinity2’), B12 = Interaction term (i.e. 214
‘Temperature by Salinity’) and a = Constant 215
216
The quadratic response surface model was fitted, in Minitab©, using a least squares loss function, 217
as a multiple regression model with five explanatory variables (temperature, salinity, quadratic 218
terms for each and interaction term). The statistical significance of each of the parameters in the 219
quadratic model and their interactions can be interpreted as follows; if there is no relationship 220
between the response variable and the explanatory variables then the response surface is flat with a 221
slope of zero. If the linear term of one explanatory variable is significant then the surface is tilted 222
along that axis. If the squared term of that same explanatory variable is also significant then the 223
surface is both tilted and curved along that axis. If the linear and squared terms of both explanatory 224
variables are both significant then the surface is tilted and curved along both axes thereby producing 225
a dome shaped surface. If the interaction term is significant then the curvature of the dome surface 226
will be asymmetrical. 227
228
Time taken to 50% mortality and estimation of optimal salinity 229
To compare the results of all the temperature/salinity experiments, a single numerical value, the 230
time to 50% survival or LT50, was calculated which described the larval and juvenile survival under 231
each of the 30 temperature/salinity combinations. Linear regressions were constructed for each of 232
the experiments using the natural log of the proportion alive against degree days. The point of 233
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intersection of the regression line and the x-axis provided the estimate of the time to 50% mortality. 234
These LT50 values were then plotted against their respective salinities for each temperature tested, 235
and a quadratic regression model was fitted. The asymptotic point on the model provided estimates 236
of the optimal salinity for survival at each temperature while the intersection with the x-axis nearest 237
the origin provided estimates of the ‘critical salinity’ i.e. the salinity that would ‘instantaneously’ 238
reduce the number of larvae to 50%. 239
240
Larval development 241
The duration to each larval stage (in days) was taken as the median development point, or the point 242
at which half of the larvae had moulted to the next stage. These values were then logged and 243
plotted against temperature and salinity. Linear regression analyses were carried out to determine 244
the effects of each experimental variable on the development rate. Declining numbers of larvae 245
over time meant that the analyses were compromised for the later developmental stages. 246
247
RESULTS 248
Larval survival in relation to temperature and salinity 249
By larval stage II (Figure 1a) 100% mortality had occurred at 9‰ salinity, across all temperatures. 250
A relatively flat-topped response was observed for all temperatures at salinities >19‰, however, 251
numbers were also reduced for combinations of high salinity (29‰ and 34‰) and low temperature 252
(10˚C and 12˚C). By larval stage III (Figure 1b) there was a decline in numbers alive at the lower 253
temperatures (i.e. <15˚C) which resulted in the formation of a slope from the lower left to the upper 254
right hand side. This pattern continued to stage IV (Figure 1c), although by stage V there was an 255
increased mortality at the higher temperature/salinity combinations, resulting in the formation of a 256
single survival peak at 15˚C and 29‰ (Figure 1d). Survival at stage VI (Figure 1e) was 257
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characterised by 2 peaks at 15˚C and 24‰, and 19˚C and 19‰. The survival peak at 15˚C and 258
29‰ had weakened by stage VII (Figure 1f) and disappeared by larval stage VIII (Figure 1g) 259
leaving a single maximum at 19˚C and 19‰. By stage IX (Figure 1h) only 6 larvae out of the 260
original 3000 were alive. No larvae achieved metamorphosis under the experimental conditions. 261
Juvenile survival in relation to temperature and salinity 262
After 100 degree days (Figure 2a) survival at the lowest temperature (10ºC) and lowest salinity 263
(9‰) was 42% while the average survival at 15 ºC, 17 ºC and 19 ºC was >90%. Survival at 200 264
degree days at 10ºC was <60% across all salinities and after 400 degree days it was <45% (Figure 265
2b and Figure 2d). At the highest temperature of 19˚C the survival at 34‰ salinity was 58% after 266
400 degree days. Highest survival (72–86%) occurred at 19–29‰ salinity and 15–17˚C. After 600 267
degree days there were no juveniles alive at 10˚C or 12˚C, and the highest survival of 66% was at 268
17˚C and 19‰ salinity (Figure 2f). This trend continued after 800 degree days with no survival 269
across all salinities at 10˚C, 12˚C and 15˚C and a single point of survival of 46% at 17˚C and 19‰ 270
salinity (Figure 2h). 271
272
A model of survival in relation to temperature and salinity 273
At zoeal stage II the fitted quadratic model accounted for 79% (adjusted R2) of the variance in the 274
survival in relation to temperature and salinity. Both salinity and salinity2 terms were significant 275
(p<0.01). Thus the general shape of the quadratic model was tilted and curved along the salinity 276
axis. At zoeal stage III both the linear salinity and salinity2 variables remained significant (p<0.05), 277
however, by stage IV only the salinity2 value was significant (p<0.05). Temperature was the only 278
significant variable at larval stage V (p<0.05), although the goodness of fit of the model was just 279
48%. Salinity2 was the most influential factor at larval stage VI (p<0.05), VII (P<0.05) and VIII 280
(p<0.05) and at the final larval stage, temperature (p<0.05), temperature2 (p<0.05) and the 281
interaction term (p<0.01) were all significant. Thus salinity was the most influential variable in 282
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determining larval survival from stage I–IV, VI, VII and VIII, while temperature was most 283
influential at stages V and IX. ANOVA showed that the quadratic model was significant (p<0.01) 284
for larval stages II–V and IX and for stage VI and VIII (p<0.05). The model was not significant for 285
larval stage VII. 286
287
The fit of the quadratic model on the survival of the juveniles was more variable than for larvae 288
with temperature, salinity and temperature2 being significant (p<0.01, adjusted R2 64%) after 100 289
degree days. Temperature (p<0.05) and salinity (p<0.01) remained significant after 200 degree 290
days, although the main response was related to salinity2 (p<0.05). After 400 degree days all 291
variables, except the interaction term, were significant (p<0.01, adjusted R2 68%). Temperature and 292
temperature2 were the most influential variables after 600 degree days (p<0.01). None of the 293
variables were significant (p>0.05, adjusted R2 36%) after 800 degree days. The quadratic model 294
was significant for the juvenile data (p<0.01) for all of the time-points tested. 295
296
Time taken to 50% mortality and estimation of optimal salinity 297
The time taken to reduce the larval numbers to 50% (LT50) (Table 1) were plotted against salinity 298
and a quadratic model was fitted to estimate the optimal salinity for larval survival at each 299
temperature (Table 2). The fit of the model was good for 10˚C, 12˚C and 15˚C with R2>0.95, 300
however, it declined at 17˚C (R2=0.58) and 19˚C (R2=0.10). It was not possible to estimate the LT50 301
for the lowest salinity of 9‰ as the time-series for these experiments did not yield sufficient data. 302
However, from the limited data it was evident that the LT50 at this salinity was 2–4 days at all 303
temperatures. Optimal salinity at 10˚C and 12˚C was estimated to be 29‰ while at 15˚C and 19˚C 304
it was 28‰. At 17˚C the optimal salinity level was 21‰. In all cases the larvae preferred salinity 305
of less than 34‰. The point where the quadratic curve intersected the x-axis represented the 306
salinity level that would ‘instantaneously’ reduce the number of larvae to 50%. At 10˚C this critical 307
salinity was ~9.5‰ while at 12˚C and 15˚C it was estimated to be 12.0‰ and 10.5‰ respectively. 308
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Values for LT50 at 17˚C and 19˚C were similar across all salinities, implying that the larvae 309
tolerated salinities as low as 14‰ for extended periods at temperatures ≥17˚C. 310
311
Juveniles had a greater tolerance of low salinity than larvae (Table 3). At 9‰ salinity and 10˚C the 312
LT50 was 111 degree days, while at 12˚C and 15˚C the LT50 was 139 degree days and 158 degree 313
days respectively. LT50 values at 9‰ salinity and 17˚C and 19˚C were 499 degree days and 621 314
degree days respectively. At 10˚C, salinity of ~5.5‰ was required to ‘instantaneously’ reduce the 315
number of juveniles to 50% (Table 4). The optimal salinity for juvenile survival at 10˚C was 26‰ 316
while at 12˚C and 15˚C it was 27‰ and 25‰. The optimal salinity at 17˚C was 23‰, although the 317
survival at this temperature was similar across all salinities. At 19˚C it was 29‰. The optimal 318
salinity of 26‰ for juvenile survival at temperatures of 10˚C, 12˚C and 15˚C was, on average, 3‰ 319
lower than that for larvae. 320
321
Larval development 322
Multiple linear regression of the log development rate on temperature and salinity showed that the 323
time to each larval stage was significantly (p<0.01) influenced by temperature but not salinity. The 324
various salinity treatments were consequently used as pseudo replicates to calculate the average 325
developmental durations at each temperature (Table 5). The relationship between temperature (T) 326
and development rate (D) to larval stage IV (Figure 3) was described by a negative power function 327
(D = 2874.9 x T -1.7978) and was significantly different for Irish and Mediterranean (Yagi & 328
Ceccaldi, 1985) populations (ANCOVA, p<0.05). 329
330
DISCUSSION 331
The results presented show that larvae and juveniles of Palaemon serratus survive and develop over 332
a broad range of salinity and temperature. Nevertheless, increased mortality rates were observed at 333
15
combinations of low temperature and low salinity. Larval survival increased with increasing 334
salinity at temperatures between 10–19˚C although survival at 34‰ was also sub-optimal. At low 335
salinity the survival of juveniles was higher than that of larvae and they also had lower salinity 336
optima. The tolerance of larval P. serratus to a broad range of salinities is not unusual among the 337
Palaemonidae and has been demonstrated in the early life stages of Palaemon xiphas and Palaemon 338
adspersus (Guerao et al., 1993). Such euryhaline physiology is evidence of adaptation by these 339
shrimp to the low salinity conditions which they encounter in coastal and estuarine habitats during 340
their early life history (Smaldon, 1993). 341
342
It is generally recognised that temperature, acting either independently or in conjunction with other 343
environmental factors, is one of the major factors affecting the survival of decapod larvae (Costlow, 344
1967; Hicks, 1973; Rochanaburanon & Williamson, 1976; Rothlisberg, 1979; Cockroft & 345
Emmerson, 1984; Preston, 1985; Anger, 1991; Brown et al., 1992; Kumlu et al., 2000; Lárez et al., 346
2000; Zacharia & Kakati, 2004; Li & Hong, 2007). However, in the present study the quadratic 347
response model showed that salinity was more important than temperature in determining survival 348
at all larval stages except stage V. In the case of juveniles the main curvature of the model changed 349
from temperature after 100 degree days to salinity after 200 degree days and back to temperature 350
after 600 and 800 degree days. 351
352
The increase in larval mortality rates after ~300 degree days may have been unrelated to 353
temperature and salinity and may instead have been due to changes in the physiology of the larvae 354
at this point in their development. Yagi et al. (1990) noted that a maximum respiration rate was 355
observed in zoeal stage IV which corresponded with a shift towards a more carnivorous diet. A 356
sudden increase in proteasic activity had previously been noted at this stage by Van Wormhoudt 357
(1973) suggesting an increase in dietary protein. In the present study 49%, 62% and 81% of the 358
larvae at 15˚C, 17˚C and 19˚C respectively were at zoeal stage IV when the mortality rates 359
16
increased. It seems likely that the additional metabolic demand of making the developmental 360
transition from zoeal stage IV resulted in the increased mortality rates observed at this time. 361
362
Genetic studies of P. adspersus and P. squilla show that gene flow is restricted between 363
neighbouring populations (Berglund & Lagercrantz, 1983). This restricted gene flow may be the 364
result of the estuarine distribution limiting offshore and alongshore dispersal of the early life stages 365
and may lead to adaptation to local environmental conditions and to different physiological 366
preferences at different latitudes (Bilton et al., 2002; Freire et al., 2003). Experiments by Yagi & 367
Ceccaldi (1985), on a Mediterranean population, found that survival was highest at high 368
temperature (21–25˚C) and high salinity (25–37‰). This contrasts with the present work where 369
larval survival was highest between 15–17˚C and optimal salinity was ≤29‰. 370
371
While larval survival rates in the present study were more influenced by salinity, larval 372
development rates were determined solely by temperature. Comparison with data from Yagi & 373
Ceccaldi (1985) showed that at a given temperature the development rate was slower for the Irish 374
than the Mediterranean population. The Irish larvae also went through nine zoeal stages whereas 375
the Mediterranean larvae metamorphosed after six. Additional larval stages can occur as a result of 376
stressful environmental conditions but typically there are 8–9 (Fincham & Figueras, 1986). 377
378
Different temperature and salinity optima for survival and development rate between Irish and 379
Mediterranean populations of P. serratus suggest that populations are adapted to local 380
environmental conditions. However, direct experimental comparisons between the two populations 381
would be necessary to discount the role of experimental variation in relation to this hypothesis. 382
Irish populations appear to have lower temperature and salinity optima for survival although their 383
development rate, at a given temperature, was slightly slower. Tolerance to lower temperatures and 384
salinities in the Irish population suggests a capacity to adapt to conditions at higher latitudes. 385
17
Together with rising ocean temperatures, due to global warming, this capacity may lead to a 386
northward expansion of P. serratus in European waters. In fact since the 1990s Irish shrimp 387
fisheries have extended from the south to the north of the country suggesting that this expansion 388
may have already begun (Kelly et al., 2009). The results also suggest that Mediterranean and Irish 389
populations may have different spawner recruit relationships. The larval development rate at a given 390
temperature is shorter in the Mediterranean population. Because larval mortality rates are very high 391
even small reductions in the duration of the larval phase can significantly increase the proportion of 392
the larval population recruiting to the juvenile phase. The efficiency of recruitment, for a given 393
spawning output, may therefore be lower at higher latitudes because temperatures are lower. 394
Recruitment may also be more variable at higher latitudes, where there is likely to be a higher 395
frequency of low salinity and low temperature events, which reduce larval survival. 396
397
The results presented here have practical implications for fisheries assessment as the incorporation 398
of environmental effects into stock-recruitment models can improve their predictive capacity. Such 399
models have been used in the management of many shrimp fisheries around the world e.g. the tiger 400
shrimp, (Penaeus esculentus) in Western Australia (Penn & Caputi, 1986), the ocean shrimp 401
(Pandalus jordani) in the Canadian Pacific (Hannah, 1993) and the white shrimp (Litopenaeus 402
setiferus) in coastal waters off Georgia, USA (Belcher & Jennings, 2004). Reducing the 403
unexplained variation in the stock-recruitment relationship will enable reference points for 404
recruitment over-fishing to be identified and increase the certainty in recruitment prediction. The 405
laboratory model described here could also be used to hindcast the likely effects of variability in 406
local temperature and salinity on shrimp recruitment. Given that the Irish shrimp fishery primarily 407
exploits the 1+ year class there is scope to include environmental effects on likely recruitment 408
success in the previous year for the management of mortality on the exploited year class. These 409
data, together with information on the relationship between development time and temperature, also 410
informs bio-physical modelling of dispersal capacity of larval populations of P. serratus. 411
18
412
ACKNOWLEDGEMENTS 413
This study formed part of a thesis submitted to the National University of Ireland, Galway in partial 414
fulfilment of the requirements for the degree of Doctor of Philosophy. We acknowledge the 415
constructive comments of Prof. Wallace Arthur. 416
417
FINANCIAL SUPPORT 418
This research was supported by the National Development Plan 2000–2006 administered by Bord 419
Iascaigh Mhara (project number 05.SM.T1.04). 420
421
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524
525
24
TABLES AND FIGURES 526
527
Fig. 1: Percentage survival (y-axis) of Palaemon serratus larvae in relation 528
to temperature (x-axis) and salinity (z-axis) at zoeal stages II-IX (charts a-h) 529
530
25
531
532
Fig. 2: Percentage survival (y-axis) of Palaemon serratus juveniles in relation to temperature (x-533
axis) and salinity (z-axis) at 100, 200, 300, 400, 500, 600, 700 and 800 degree days (charts a-h) 534
535
536
26
537
Fig. 3: Development rate of Irish and Mediterranean Palaemon serratus larvae to zoeal stage IV at 538
various temperatures 539
540
27
541
Table 1: Linear regression coefficients for natural log of proportion of Palaemon serratus larvae 542
alive (y-axis) against time (x-axis) and time required to reduce initial numbers to 50% 543
Temp.
(˚C)
Salinity
(‰)
Slope Constant R2 N Days
to 50%
Degree Days
to 50%
10 9 - - - 1 - -
10 14 0.2634 -4.6108 0.90 12 17.5 175.0
10 19 0.1776 -5.0022 0.90 21 28.2 281.7
10 24 0.1066 -3.8686 0.93 29 36.3 362.9
10 29 0.0788 -3.3775 0.88 29 42.9 428.6
10 34 0.0781 -2.7614 0.84 28 35.4 353.6
12 9 - - - 1 - -
12 14 0.8448 -6.1332 0.99 4 7.3 87.1
12 19 0.3523 -4.9765 0.90 14 14.1 169.5
12 24 0.1917 -4.6177 0.98 20 24.1 289.1
12 29 0.1163 -3.1675 0.93 20 27.2 326.8
12 34 0.1261 -2.8951 0.89 20 23.0 275.5
15 9 - - - 1 - -
15 14 0.6852 -6.3455 0.91 5 9.3 138.9
15 19 0.1570 -2.5924 0.85 19 16.5 247.7
15 24 0.1675 -4.0540 0.94 19 24.2 363.0
15 29 0.1749 -4.1410 0.91 19 23.7 355.1
15 34 0.1755 -3.7118 0.87 15 21.1 317.2
17 9 - - - 1 - -
17 14 0.2196 -4.1683 0.89 15 19.0 322.7
17 19 0.1734 -3.1603 0.85 15 18.2 309.8
17 24 0.3280 -6.0763 0.91 13 18.5 314.9
17 29 0.3403 -6.7046 0.88 11 19.7 334.9
17 34 0.3195 -4.8069 0.90 11 15.0 255.8
19 9 - - - 1 - -
19 14 0.2095 -2.6623 0.94 15 12.7 241.4
19 19 0.1613 -3.0648 0.96 15 19.0 361.0
19 24 0.2235 -3.0377 0.92 14 13.6 258.2
19 29 0.3346 -5.1921 0.95 14 15.5 294.8
19 34 0.2771 -4.5359 0.95 15 16.4 311.0
544
545
28
Table 2: Quadratic regression coefficients for LT50 in degree days against salinity to estimate 546
optimal and critical values for Palaemon serratus larval survival 547
Temp.
(˚C)
N Squared
Term
Linear
Term
Constant R2 Critical
Salinity (‰)
Optimal
Salinity (‰)
10 5 -1.08 62.04 -490.91 0.96 9.5 29
12 5 -1.00 58.57 -551.56 0.96 12.0 29
15 5 -1.19 66.42 -564.46 0.98 10.5 28
17 5 -0.34 13.97 182.89 0.58 - 21
19 5 -0.19 10.70 157.02 0.10 - 28
548
549
29
550
Table 3: Linear regression coefficients for natural log of proportion of Palaemon serratus juveniles 551
alive (y-axis) against time (x-axis) and time required to reduce initial numbers to 50% 552
Temp.
(˚C)
Salinity
(‰)
Slope Constant R2 N Days
to 50%
Degree Days
to 50%
10 9.0 0.1985 -2.2087 0.93 15 11.1 111.3
10 14.0 0.0706 -1.2545 0.81 25 17.8 177.7
10 19.0 0.0580 -1.7625 0.92 24 30.4 303.9
10 24.0 0.0664 -1.8329 0.77 25 27.6 276.0
10 29.0 0.0504 -1.7859 0.73 25 35.4 354.3
10 34.0 0.0630 -1.5937 0.78 25 25.3 253.0
12 9.0 0.2720 -3.1466 0.94 12 11.6 138.8
12 14.0 0.1040 -1.6413 0.76 13 15.8 189.4
12 19.0 0.2450 -5.6522 0.90 6 23.1 276.8
12 24.0 0.1267 -2.7149 0.77 13 21.4 257.1
12 29.0 0.1460 -2.8018 0.80 13 19.2 230.3
12 34.0 0.1171 -2.5218 0.70 13 21.5 258.4
15 9.0 0.1158 -1.2204 0.79 23 10.5 158.1
15 14.0 0.0705 -2.8499 0.82 21 40.4 606.4
15 19.0 0.0890 -3.9883 0.90 21 44.8 672.2
15 24.0 0.0917 -3.9892 0.97 19 43.5 652.5
15 29.0 0.0965 -3.8746 0.94 21 40.2 602.3
15 34.0 0.1073 -4.4550 0.93 20 41.5 622.8
17 9.0 0.0722 -2.1185 0.88 30 29.3 498.8
17 14.0 0.0794 -2.5569 0.91 32 32.2 547.4
17 19.0 0.0664 -3.1859 0.98 32 48.0 815.7
17 24.0 0.0737 -2.8402 0.98 32 38.5 655.1
17 29.0 0.1009 -4.0969 0.98 32 40.6 690.3
17 34.0 0.0921 -2.9454 0.93 32 32.0 543.7
19 9.0 0.1295 -4.2295 0.97 26 32.7 620.5
19 14.0 0.1105 -2.2221 0.96 22 20.1 382.1
19 19.0 0.1039 -1.8848 0.94 22 18.1 344.7
19 24.0 0.1162 -3.2704 0.97 28 28.1 534.7
19 29.0 0.1008 -3.1710 0.97 27 31.5 597.7
19 34.0 0.1057 -3.0960 0.95 28 29.3 556.5
553
554
30
555
Table 4: Quadratic regression coefficients for LT50 in degree days against salinity to estimate 556
optimal and critical values for Palaemon serratus juvenile survival 557
Temp.(˚C) N Squared
Term
Linear
Term
Constant R2 Critical
Salinity (‰)
Optimal
Salinity (‰)
10 5 -0.74 38.57 -189.28 0.86 5.5 26
12 5 -0.41 21.49 -19.31 0.82 - 27
15 5 -1.86 93.05 -453.10 0.82 - 25
17 5 -1.36 61.43 -33.96 0.67 - 23
19 4 -2.31 136.54 -1413.60 0.99 - 29
558
559
Table 5: Average cumulative duration (days) of Palaemon serratus to each larval stage in relation 560
to temperature (Number of experimental observations, Standard Deviation) 561
Temp.
(˚C)
ZI-ZII
ZI-ZIII
ZI-ZIV
ZI-ZV
ZI-ZVI
ZI-ZVII
ZI-ZVIII
ZI-ZIX
10 17.4
(5, 1.7)
35.5
(4, 2.5)
49.3
(3, 1.2)
- - - - -
12 14.0
(4, 0.0)
25.5
(4, 4.7)
32.7
(3, 4.2)
37.3
(3, 2.3)
- - - -
15 8.8
(5, 1.8)
15.5
(4, 1.9)
19.5
(4, 1.0)
27.0
(4, 2.0)
30.0
(3, 0.0)
35.0
(2, 1.4)
38.0
(1, -)
-
17 6.0
(5, 0.0)
10.8
(5, 1.1)
17.6
(5, 0.9)
20.8
(5, 1.8)
26.7
(3, 1.2)
27.0
(2, 1.4)
29.0
(2, 1.4)
-
19 4.8
(5, 1.1)
8.4
(5, 2.2)
15.6
(5, 2.2)
20.0
(5, 0.0)
21.6
(5, 0.9)
24.0
(5, 0.0)
26.0
(5, 1.4)
28.0
(2, -)
562